Seasonal Changes in Zoanthus spp. in the Infra-LittoralZone at Taisho Lava Field, Sakurajima, Kagoshima, Japan

Shusuke ONO, James Davis REIMER and Junzo TSUKAHARA

Abstract

Changes in Zoanthus spp. cover and polyp number were recorded by transect survey at Taisho Lava Field,Sakurajima, Kagoshima, Japan (N31°35’, E135°35’) for 30 months between May 1980 to October 1982. Inaddition, lab experiments were conducted to investigate changes in polyps, Zoanthus’ gonads and zooxanthellaenumber at different seawater temperatures. Our results indicate that Zoanthus polyps grow during summer andautumn, and experience a decrease in size during winter and spring. Polyps close during periods with low wintertemperatures, and zooxanthellae activity and concentration also decrease, perhaps due to the winter growth inmany types of algae above polyps and the appearance of diatoms on polyps themselves. In addition, volcanic ashfrom the nearby active volcanic cone of Sakurajima also has a negative effect on Zoanthus polyps.

Key Words: Zoanthus, seawater temperature, seasonal changes, volcanic ash, diatom

Introduction

Zoanthus spp. (Brachcnemia, Zoanthidae) are an encrusting anemone-like group that formcolonies of polyps, and are found in Japan from mid-Honshu south at depths from the lowtide line and below. To investigate changes in the infra-littoral zone in corals andCnidarians at Sakurajima’s Taisho study site, Zoanthus was selected as the subject speciesfor an on-going transect survey, changes in the environment are easily seen in Zoanthuspolyps, although until now research has been scarce (BABCOCK and RYLAND, 1990).

Besides Zoanthus spp., Stereonephthya, Dendronephthya, Acropora, Favia, Porites,Pavona, Montipora, and Hydnophora species are all readily visible at the rocky TaishoLava Field site, located in Sakurajima, Kagoshima, Japan (HIRATA and OSAKO, 1969).Previous research has shown that these and other species are influenced not only byexpected environmental factors, such as seawater temperature, but that volcanic ash-fallfrom the nearby Sakurajima volcanic cone also impacts the Taisho Lava Field infra-littoralenvironment (ONO and TSUKUHARA, 2000).

Data collected from transect surveys for this study showed that of all the species at theTaisho site, Zoanthus especially displayed large variability from season to season. Labora-tory experiments were carried out to investigate possible reasons behind this variability.Identification of Zoanthus to the species level is extremely difficult (BORNEMANN, 1998),

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Kagoshima University, Faculty of Science, Department of Chemistry and BioScience, Kagoshima, 890-0065, Japan

and therefore identification was made only to the genus level. Further research investigat-ing what species of Zoanthus are present at the Taisho site is necessary.

Materials and Methods

The subject study species Zoanthus forms colonies consisting of many individual polyps(Fig. 1). Polyps are on average 5~7 mm in diameter across the oral disk, and have a lengthof 10~30 mm. Inside the polyp in the internal gastro-intestinal cavity innumerableendosymbiotic Symbiodinium spp. zooxanthellae are present.

The study site at the Taisho Lava Field is located on the western shore of Sakurajima,Kagoshima (Fig. 2). The site was formed during the Taisho Eruption of Sakurajima in1914, and the area still receives regular dustings of volcanic ash from the active Sakurajimavolcano’s eruptions (FUKUYAMA and ONO, 1981). The study site is in a small bay and is20 × 50 m. Four stations (Stations 1~4) were chosen at depths of 1~3 m, and every monthfrom May 1980 to October 1982 (30 months total) these areas were surveyed using a 50× 50 cm transect. Coverage of Zoanthus and other species were noted. At the same time,samples of Zoanthus were collected from depths of 1~3 m near the transect stations duringeach survey, and stored in the laboratory at -60℃. The samples were used to examinepolyp size and zooxanthellae condition.

To investigate polyp growth and shape, samples were collected during August fromvarious places in the study site as entire portions of a colony (still connected with stolons)to prevent unwanted mortality. Individual polyps were taken from the colony sample, and

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Fig. 1 Colony of Zoanthus aff. pacificus in natural condition in the infra-littoral zoneat Taisho Lava Fields, Sakurajima. Zoanthus polyps are 5~7 mm in diameterwhen open, and have a length of 10-30 mm, containing innumerablezooxanthellae in the gastro-intestinal cavity.

the samples were placed in salt water tanks on glass plates in a laboratory under twodifferent controlled conditions; (1) L:D = 12:12 hrs, 4000 lux, 22℃- corresponding to thestudy site average spring and autumn temperature, and (2) same as (1) with a temperatureof 16℃, which is the average seawater temperature in winter. Ten individual polyps wereplaced in each temperature regime tank. Individual polyps were also examined, and oraldisk diameter, length, stolon count, and polyp count were recorded. No food was given tosamples before, during, and after the experiments were conducted.

Further, to investigate gonad changes, every month from March 2000 to April 2001(every week between April and July 2000) several polyps were collected from near Station2 and placed in Bouin’s fixative solution. Samples were then mounted in paraffin andstained with Azan’s staining solution. For the scanning electron microscopic study of theultrastructural surface of the polyps samples were fixed in glutaraldehyde and OsO4,dehydrated, dried, and coated with platinum. A Hitachi S-4100 scanning electron micro-scope was used.

Results

Seasonal changes in Zoanthus coverStation 1 is located 10 m from shore, at a depth of 1 m. The bottom consists mainly of alarge volcanic rock approximately 3 m in diameter. Compared with stations 2 and 3, station

43Seasonal Changes in Zoanthus spp. in the Infra-Littoral Zone at Taisho Lava Field, Sakurajima, Kagoshima, Japan

Fig. 2 Map of study site: Taisho Lava Field, Sakurajima, Kagoshima, Japan. E.L.W.S.= Extreme Low Water Spring tide line, E.H.W.S. = Extreme High WaterSpring tide line, St. = Station.

1’s water temperature and wave height, are more variable. Compared with other stations,Zoanthus cover at Station 1 was consistently higher throughout the course of the transectsurvey. Stations 2, 3, and 4 are located approximately at depths of 2.5, 3, and 3 m, and 15,17, and 18 m from infra-littoral line, respectively. Zoanthus cover at Stations 2, 3, and 4was generally below 40%..

As shown in Figure 3, Zoanthus cover increased between August and December, anddecreased from December to August. During the last part of August in 1982 Sakurajimaerupted heavily several times, resulting in extremely heavy ash-fall (5.5 kg/m2 /day)(KAGOSHIMA METEOROLOGICAL STATION: PERSONAL COMMUNICATION). At stations 2 and3, where wave influence is low, up to 3~5 cm of ash covered Zoanthus. This resulted inthe cover of Zoanthus decreasing from 45.5 % in July 1982 to 10.1% in October 1982.

Figure 4 shows colony numbers and size data from Stations 1~4. Colony size wasdivided into five sizes; less than 0.25 cm2, 0.25~6.25 cm2, 6.25~25.0 cm2, 25.0~100 cm2,and over 100 cm2. The number of small (0.25 cm2 or less) colonies (i.e. new colonies)increased between May and September. From September to November the number ofcolonies less than 0.25 cm2 decreased, and the number of colonies in the range of 0.25~6.25cm2 increased. From November to April the number of all colonies decreased.

The length of polyps was investigated (Fig. 5) by counting approximately 200~300polyps per month. Small polyps with a length of less than 5 mm were very common

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Fig. 3 Changes in Zoanthus cover, May 1980~Oct. 1982.

45Seasonal Changes in Zoanthus spp. in the Infra-Littoral Zone at Taisho Lava Field, Sakurajima, Kagoshima, Japan

Fig. 4 Seasonal changes of Zoanthus colonies at Stations 1~4 by number and colonysize, May 1980~Oct. 1982.

between September and February.

Seasonal frequency of macro-algae and diatomsA strong seasonal variation was seen in macro-algae and diatom (Fig. 6a, b, c) cover.Sargassum, Colpomenia sinuosa, and other species of macro-algae grow to approach 100%cover during the winter to spring period (Fig. 7). In areas above Zoanthus polyps thismacro-algae cover appears to be especially dense. Diatoms appeared during winter andspring covering Zoanthus polyps.

Seasonal frequency of inactive zooxanthellaeWinter sea water temperatures at the Taisho Lava Field reach a low of approximately 15~16℃, and at this temperature Zoanthus’ oral disks close, which was observed both in thefield and in the lab. As seen in Figure 8, the ratio of inactive zooxanthellae generallyincreased from winter (January) to summer (June). This is reflected in the decreasedhealthiness in the zooxanthellae, and lower chlorophyll concentrations (personal data).When macro-algae cover is 100% during May (personal data), chlorophyll-lesszooxanthellae account for 79% of all zooxanthellae, while in September this numberdecreases to 12.2% .

Zoanthus temperature and polyp growth experimentsFigure 9 shows the number of stolons of Zoanthus kept in tanks at results from Zoanthuspolyps kept in lab tanks at 16℃ and 22℃ over 10 weeks. At 16℃ , no new stolonsdeveloped, and all polyps closed their oral disks. No polyps were seen to attach themselves

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Fig. 5 Changes in Zoanthus polyp length (mm) by month, 1981.

47Seasonal Changes in Zoanthus spp. in the Infra-Littoral Zone at Taisho Lava Field, Sakurajima, Kagoshima, Japan

Fig. 6 Zoanthus polyps in winter(a) Zoanthus polyps in the infra-littoral zone, February 2000. Polyps are in

typical winter condition, with oral disks closed.(b) Zoanthus polyp epidermis under electron microscope, February 2000.

Small disk-like objects are diatoms.(c) Detail of (b). The presence of many diatoms on the surface of the

Zoanthus polyps is clearly evident.Both (b) and (c) were taken with a scanning electron microscope. Scale isshown on the photographs.

to the glass plate substrate, while at 22℃ polyps attached themselves to the substrate. Inaddition, at 22℃, stolons were seen to develop at 28 days from the start of the experiment,and after approximately 6 weeks all polyps showed division of the stolon. However, evenafter 200 days, no new formation or division of polyps was seen.

Zoanthus reproductionBased on the monthly (and weekly from April to July 2000) cross-sections of Zoanthus,

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Fig. 7 Changes in macro-algae cover at Stations 1~4, May 1980 to Oct. 1982.

Fig. 8 Changes in inactive zooxanthellae over 1 year (1981) at the study site.

eggs appear inside polyps from June, and grow bigger until being released during the largesttides of July (Fig. 10a). After spawning no eggs were to be seen in the cross section untilthe following June. Spermatogenesis began at the beginning of July, when earlyspermatogenia were seen to develop into spermatocytes, followed by spermatids, and finallydeveloped into sperm (Fig. 10b). Sperm were released at the same time as the eggs duringthe big summer tides. After spawning, vesicles shrank until they were not visible. Based onthese observations it is likely that fertilized embryos appear after the July spawning, leadingto the increase in small <0.25 cm2 polyps seen from September.

Discussion

The Effect of Light and Volcanic AshThe growth cycle of Zoanthus polyps can be divided into two different phases, an expansionphase from summer to autumn, and a contraction phase from late autumn to early summer.Sargassum, Colpomenia sinuosa, and other species of macro-algae grow to approach 100%cover from winter to spring. Diatoms were seen to grow on individual Zoanthus polyps.

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Fig. 9 Changes in Zoanthus stolon number L:D =12:12 hr, 4000 lux, 16℃ and 22℃,over 10 weeks.

Seasonal Changes in Zoanthus spp. in the Infra-Littoral Zone at Taisho Lava Field, Sakurajima, Kagoshima, Japan

Undoubtedly this cover influences the growth and fitness of Zoanthus, both on the colonyand polyp level.

Based on the results, it seems safe to say that at low sea water temperatures Zoanthuspolyps close their oral disks, decrease in size and number, and that endosymbioticzooxanthellae decrease their activity, while macro-algae and diatom cover increase. Athigher temperatures, polyps enter a state of growth and activity, characterized by anopening of oral disks, development and growth of stolons and polyps, and the appearanceof small, new polyps, and spawning may occur during extreme summer tides. As well, thesesummer conditions correspond with a decrease in macro-algae and diatom cover. Inaddition, Zoanthus’ reliance on light may be further demonstrated by the fact that very fewplankton and other types of potential food sources were seen inside the gastro-intestinal

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Fig. 10 Zoanthus polyps’ gonads(a) Ovaries of a sample polyp one week before release of eggs and sperm,

July 2000. Diameter at widest point of ovaries, approximately 100~150μm; diameter at narrowest point, 70~100μm. Scale bar: 100μm.

(b) Sperm bundles one week before release of eggs and sperm, July 2000.Each bundle is approximately 100μm in diameter.

Both photos were taken with a light microscope at 100 ×. Scale bar: 100μm.

cavity during the course of the experiment. In fact, it is easy to suggest that Zoanthus almostcompletely relies upon its zooxanthellae for energy. Thus, in times when light levels arenot sufficient, Zoanthus cannot grow nor expand.

Due to the fact that the study site is located in a small bay removed somewhat fromcurrents and other influences, volcanic ash should have a strong effect on organisms livingin the infra-littoral zone of the study area (ONO et al., 2002, in preparation). During the lastpart of August 1982 there were several large eruptions from Sakurajima volcano. 3~5 cmof ash covered Zoanthus and other encrusting species. In the months after the eruption deadZoanthus (as well as other species) were seen at the study site. Figure 11 shows the ash-fallat sites near the Taisho field site (ANNUAL REPORT OF KAGOSHIMA PREFECTURE

EMERGENCY OFFICE, 1998). Based on our observations and results, it is safe to say thatvolcanic ash has a harsh and debilitating effect on Zoanthus.

The Effect of Seawater TemperatureLow seawater temperatures result in the closure of polyps’ oral disks, as well as the growthof macro-algae and diatoms. This causes a decrease in the activity of endosymbioticzooxanthellae, and a stoppage and/or reversal in Zoanthus growth. Based on these results,one could expect to find Zoanthus in areas where winter sea temperatures do not go muchbelow 16℃. This hypothesis merits further investigation.

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Fig. 11 Changes in volcanic ash-fall from 1978 to 1982 at three sites near the studysite at Sakurajima, Kagoshima.

Seasonal Changes in Zoanthus spp. in the Infra-Littoral Zone at Taisho Lava Field, Sakurajima, Kagoshima, Japan

Worldwide, widespread coral bleaching was observed in 1998, likely due highseawater temperatures (TSUCHIYA, 1999). In Japan, Okinawan coral reefs suffered heavybleaching damage (SUGIYAMA et al., 1999; YAMAZATO, 1999). As noted in separateresearch (ONO et al., 2001) Sakurajima also showed signs of bleaching.

As worldwide temperature increases are expected in the coming years, one can expectthat the frequency of coral bleaching will also become more intense, and therefore furtherresearch into the effect of temperature and the environment on Zoanthus and other speciesof encrusting corals has become more necessary than ever.

Acknowledgments

The authors wish to thank Professor Emeritus Yoshiko Kakinuma and Professor ToshioIchikawa for their help and advice during the course of the research. For gracefullyproviding volcanic ash fall data, our sincere thanks go to the Kagoshima PrefecturalEmergency Office.

References

BABCOCK, R.C., and RYLAND J.S. 1990. Larval development of a tropical zoanthid(Protopalythoa sp.) Invertebrate Reproduction and Development, 17:3 229-236.

BORNEMANN, E. 1998 http://www.aquarium.net/0198/0198_1.shtmlFUKUYAMA, H., and ONO, K. 1981. Geological map of Sakurajima volcano. Geological

Survey of Japan, 1-8. (in Japanese)HIRATA, K., and OSAKO, Y. 1969. Marine park report in Kagoshima Bay. Kagoshima

Prefecture Report, 9-19. (in Japanese)ONO, S., REIMER, J.D., and TSUKUHARA, J. 2002. An ecological study on the dynamics of

Zoanthus spp. and macrobenthos in the infra-littoral zone at the Taisho Lava Field,Sakurajima, Kagoshima, Japan. (in preparation)

ONO, S., and TSUKUHARA, J. 2000. An ecological study on the dynamics of soft coralcommunities in the infra-littoral zone at the Taisho Lava Field, Sakurajima, Kagoshima,Japan. Shizen-aigo 26: 14-17. (in Japanese)

SUGIYAMA K., IRYU, Y., and NAKAMORI, T. 1999. Coral bleaching, geological rangers, andadaptation to high sea surface temperature. Galaxea JCRS 1: 89-95.

TSUCHIYA, M. 1999. Warning from the coral reefs. Galaxea JCRS 1: 27-29.YAMAZATO, M. 1999. Coral bleaching in Okinawa, 1980 vs. 1998. Galaxea JCRS 1: 83-87.

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